The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes.
The macronuclear genome of the ciliate Oxytricha trifallax displays an extreme and unique eukaryotic genome architecture with extensive genomic variation. During sexual genome development, the expressed, somatic macronuclear genome is whittled down to the genic portion of a small fraction (∼5%) of i...
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oai:doaj.org-article:2c997db6921e48499101458b87b256412021-11-18T05:37:16ZThe Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes.1544-91731545-788510.1371/journal.pbio.1001473https://doaj.org/article/2c997db6921e48499101458b87b256412013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23382650/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885The macronuclear genome of the ciliate Oxytricha trifallax displays an extreme and unique eukaryotic genome architecture with extensive genomic variation. During sexual genome development, the expressed, somatic macronuclear genome is whittled down to the genic portion of a small fraction (∼5%) of its precursor "silent" germline micronuclear genome by a process of "unscrambling" and fragmentation. The tiny macronuclear "nanochromosomes" typically encode single, protein-coding genes (a small portion, 10%, encode 2-8 genes), have minimal noncoding regions, and are differentially amplified to an average of ∼2,000 copies. We report the high-quality genome assembly of ∼16,000 complete nanochromosomes (∼50 Mb haploid genome size) that vary from 469 bp to 66 kb long (mean ∼3.2 kb) and encode ∼18,500 genes. Alternative DNA fragmentation processes ∼10% of the nanochromosomes into multiple isoforms that usually encode complete genes. Nucleotide diversity in the macronucleus is very high (SNP heterozygosity is ∼4.0%), suggesting that Oxytricha trifallax may have one of the largest known effective population sizes of eukaryotes. Comparison to other ciliates with nonscrambled genomes and long macronuclear chromosomes (on the order of 100 kb) suggests several candidate proteins that could be involved in genome rearrangement, including domesticated MULE and IS1595-like DDE transposases. The assembly of the highly fragmented Oxytricha macronuclear genome is the first completed genome with such an unusual architecture. This genome sequence provides tantalizing glimpses into novel molecular biology and evolution. For example, Oxytricha maintains tens of millions of telomeres per cell and has also evolved an intriguing expansion of telomere end-binding proteins. In conjunction with the micronuclear genome in progress, the O. trifallax macronuclear genome will provide an invaluable resource for investigating programmed genome rearrangements, complementing studies of rearrangements arising during evolution and disease.Estienne C SwartJohn R BrachtVincent MagriniPatrick MinxXiao ChenYi ZhouJaspreet S KhuranaAaron D GoldmanMariusz NowackiKlaas SchotanusSeolkyoung JungRobert S FultonAmy LySean McGrathKevin HaubJessica L WigginsDonna StortonJohn C MateseLance ParsonsWei-Jen ChangMichael S BowenNicholas A StoverThomas A JonesSean R EddyGlenn A HerrickThomas G DoakRichard K WilsonElaine R MardisLaura F LandweberPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 11, Iss 1, p e1001473 (2013) |
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Biology (General) QH301-705.5 |
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Biology (General) QH301-705.5 Estienne C Swart John R Bracht Vincent Magrini Patrick Minx Xiao Chen Yi Zhou Jaspreet S Khurana Aaron D Goldman Mariusz Nowacki Klaas Schotanus Seolkyoung Jung Robert S Fulton Amy Ly Sean McGrath Kevin Haub Jessica L Wiggins Donna Storton John C Matese Lance Parsons Wei-Jen Chang Michael S Bowen Nicholas A Stover Thomas A Jones Sean R Eddy Glenn A Herrick Thomas G Doak Richard K Wilson Elaine R Mardis Laura F Landweber The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| description |
The macronuclear genome of the ciliate Oxytricha trifallax displays an extreme and unique eukaryotic genome architecture with extensive genomic variation. During sexual genome development, the expressed, somatic macronuclear genome is whittled down to the genic portion of a small fraction (∼5%) of its precursor "silent" germline micronuclear genome by a process of "unscrambling" and fragmentation. The tiny macronuclear "nanochromosomes" typically encode single, protein-coding genes (a small portion, 10%, encode 2-8 genes), have minimal noncoding regions, and are differentially amplified to an average of ∼2,000 copies. We report the high-quality genome assembly of ∼16,000 complete nanochromosomes (∼50 Mb haploid genome size) that vary from 469 bp to 66 kb long (mean ∼3.2 kb) and encode ∼18,500 genes. Alternative DNA fragmentation processes ∼10% of the nanochromosomes into multiple isoforms that usually encode complete genes. Nucleotide diversity in the macronucleus is very high (SNP heterozygosity is ∼4.0%), suggesting that Oxytricha trifallax may have one of the largest known effective population sizes of eukaryotes. Comparison to other ciliates with nonscrambled genomes and long macronuclear chromosomes (on the order of 100 kb) suggests several candidate proteins that could be involved in genome rearrangement, including domesticated MULE and IS1595-like DDE transposases. The assembly of the highly fragmented Oxytricha macronuclear genome is the first completed genome with such an unusual architecture. This genome sequence provides tantalizing glimpses into novel molecular biology and evolution. For example, Oxytricha maintains tens of millions of telomeres per cell and has also evolved an intriguing expansion of telomere end-binding proteins. In conjunction with the micronuclear genome in progress, the O. trifallax macronuclear genome will provide an invaluable resource for investigating programmed genome rearrangements, complementing studies of rearrangements arising during evolution and disease. |
| format |
article |
| author |
Estienne C Swart John R Bracht Vincent Magrini Patrick Minx Xiao Chen Yi Zhou Jaspreet S Khurana Aaron D Goldman Mariusz Nowacki Klaas Schotanus Seolkyoung Jung Robert S Fulton Amy Ly Sean McGrath Kevin Haub Jessica L Wiggins Donna Storton John C Matese Lance Parsons Wei-Jen Chang Michael S Bowen Nicholas A Stover Thomas A Jones Sean R Eddy Glenn A Herrick Thomas G Doak Richard K Wilson Elaine R Mardis Laura F Landweber |
| author_facet |
Estienne C Swart John R Bracht Vincent Magrini Patrick Minx Xiao Chen Yi Zhou Jaspreet S Khurana Aaron D Goldman Mariusz Nowacki Klaas Schotanus Seolkyoung Jung Robert S Fulton Amy Ly Sean McGrath Kevin Haub Jessica L Wiggins Donna Storton John C Matese Lance Parsons Wei-Jen Chang Michael S Bowen Nicholas A Stover Thomas A Jones Sean R Eddy Glenn A Herrick Thomas G Doak Richard K Wilson Elaine R Mardis Laura F Landweber |
| author_sort |
Estienne C Swart |
| title |
The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| title_short |
The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| title_full |
The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| title_fullStr |
The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| title_full_unstemmed |
The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| title_sort |
oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2013 |
| url |
https://doaj.org/article/2c997db6921e48499101458b87b25641 |
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